Global Ecology Ecology and and Biogeography, Biogeography, (Global (Global Ecol. Biogeogr.)Ecol. Biogeogr.)(2015) () 25, 324–334 RESEARCH Marine protected areas are insufficient PAPER to conserve global marine plant diversity Barnabas H. Daru* and Peter C. le Roux Department of Plant Sciences, University of ABSTRACT Pretoria, Pretoria, South Africa Aim Marine plants are only incidentally included in conservation efforts for marine biodiversity. Here, for the first time, we apply phylogenetic methods to marine macrophytes (mangroves and seagrass species) to test for gaps in the current conservation network by identifying global diversity hotspots for these plant groups, and assess the degree to which hotspots are represented within the current network of marine protected areas (MPAs). Location Global. Methods We calculated five metrics of marine plant diversity: phylogenetic diver- sity, species richness, species endemism, phylogenetic endemism and ‘evolutionary distinctiveness and global endangerment’ (EDGE). Results Overall, the diversity of marine plants was poorly represented by current MPAs. Different measures of diversity showed spatial mismatch, demonstrating how strategies that maximize one diversity measure may be inefficient at protecting other facets of marine plant biodiversity. However, complementarity analyses revealed that complete representation can be achieved very efficiently with few additional locations. Main conclusions Our study highlights the need for an integrative approach to conserve both the species diversity and phylogenetic diversity of marine plants. While MPAs are a valuable instrument for conserving marine biodiversity, we now face the challenge of increasing coverage to protect other branches of the marine *Correspondence: Barnabas H. Daru, tree of life. Department of Plant Sciences, University of Keywords Pretoria, Private Bag X20, Hatfield 0028, Pretoria, South Africa. Biodiversity hotspots, complementarity analyses, mangroves, marine plants, E-mail: [email protected] phylogenetic diversity, protected areas, seagrasses. 2007; Mellin et al., 2011). Indeed, there is inconsistent support INTRODUCTION for the use of cross-taxon surrogates (where well-studied taxo- Although the system of marine protected areas (MPAs) remains nomic groups can effectively serve as surrogates to represent the most significant instrument for managing and protecting patterns of diversity of more poorly known taxa; Rodrigues & the biological resources of the oceans, MPAs were initially Brooks, 2007) in conservation planning. For example, some designed for preserving fish stocks, coral reefs and other animal studies have suggested that environmental factors may be a more resources (Gaines et al., 2010). This suggests that non-target efficient proxy for biodiversity (e.g. Tittensor et al., 2010; Beier taxa and their associated habitats are often only incidentally & de Albuquerque, 2015), while others have found spatial mis- included in current efforts to protect biodiversity in the marine matches between various taxonomic groups (e.g. Zupan et al., realm. Moreover, the major groups of conservation focus in the 2014), suggesting that usefulness of cross-taxon surrogates may marine world, mainly marine mammals, coral reefs and fish, depend on the scale or context of the study (e.g. Ferrier & may not fully represent the diversity of other taxa due to their Watson, 1997; Rodrigues & Brooks, 2007). As a result, explicit different evolutionary histories (see, e.g., Rodrigues & Brooks, examination of the representation of non-target species within © 2015 John Wiley & Sons LtdDOI: 10.1111/geb.12412 10.1111/geb.12412 324 VC 2015http://wileyonlinelibrary.com/journal/geb John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/geb1 B. H. Daru and P. C. le Roux Marine plant diversity hotspots MPAs is necessary to assess their protection status. Moreover, et al., 2004), through the incorporation of phylogenetic infor- given that marine species are more prone to extinction than mation and the application of complementarity methods. previously thought (McKinney, 1998), due to human pressures With this aim, we develop an integrative approach to assess (Roberts et al., 2002; McCauley et al., 2015), it is critical to deter- current marine protection efforts by combining spatial analyses mine the extent to which MPAs conserve species of other dis- with taxonomic and phylogenetic techniques to identify tinct evolutionary branches of the marine tree of life (Murdoch hotspots for two important aquatic and semi-aquatic plant et al., 2007). groups: seagrasses and mangroves. These two groups are the A common approach to designating areas of conservation only vascular plants inhabiting coastal environments and estu- priority is via hotspots, i.e. geographical clusters of biodiversity aries world-wide that can live exclusively in the marine environ- (Myers et al., 2000; see also Orme et al., 2005). In the marine ment without any freshwater input; they present an excellent realm, biodiversity hotspots have been defined using taxo- opportunity to explore the degree of protection of a (usually) nomic metrics such as species richness (SR), endemism or risk non-target group in the current marine conservation network. of extinction (Roberts et al., 2002; Davidson et al., 2012), Both seagrasses and mangroves are keystone species, having a thereby missing out on the full richness of biodiversity cap- disproportionately strong influence on co-occurring species, tured by phylogenetic information (Faith, 1994; Williams et al., largely via ecosystem engineering effects. Seagrasses (72 species; 1994). Even with simple taxonomic metrics of diversity, spatial Hemminga & Duarte, 2000) and mangroves (70 species; mismatches between individual taxonomic metrics have often Spalding et al., 1997) play critical roles in sediment accumula- been reported (Roberts et al., 2002), suggesting that current tion, carbon sequestration and nutrient cycling, act as a nursery marine hotspots are insufficient to capture even species-level for many fish and invertebrates and anchor several foodwebs diversity. (Beck et al., 2001; Green & Short, 2003). Cumulatively, their Some lineages differ markedly in the amount of evolutionary ecosystem services are valued at c. USD 2 trillion annually history they embody (Vane-Wright et al., 1991; Faith, 1992). As (Costanza et al., 1997; Field et al., 1998; Waycott et al., 2009). We a result, integrating phylogenetic information is an important refer to these two ecological groups collectively as ‘macrophytes’. advance in conservation (Bininda-Emonds et al., 2000), allow- Here, for the first time, we apply phylogenetic methods to ing reserve networks to be planned that maximize the amount of marine macrophytes to test for gaps in the current conservation unique evolutionary history that is captured (Sechrest et al., network. Specifically, we address three objectives. First, we map 2002; Jetz et al., 2014). For instance, considering phylogenetic patterns and hotspots (defined as the top 2.5% of cells) of SR, metrics in conservation prioritization allows the identification PD, corrected weighted endemism (CWE), phylogenetic of areas harbouring evolutionarily distinct lineages, i.e. once- endemism (PE) and evolutionary distinctiveness and global diverse lineages that are now reduced due to historical extinc- endangerment (EDGE) for each taxonomic group. Second, we tions, or of regions with recently diversified clades that may explore the complementarity of macrophyte SR and PD in rep- represent centres of speciation (e.g. Forest et al., 2007). resenting all species/branch lengths in as small an area as pos- Phylogenetic metrics, including phylogenetic diversity (PD), sible. Finally, we evaluate the degree to which the current global phylogenetic endemism and evolutionary distinctiveness and network of MPAs covers macrophyte hotspots. global endangerment, all measure different facets of evolution- ary diversity (Isaac et al., 2007; Cadotte et al., 2010) and have METHODS been used to delineate biodiversity hotspots, but only in the terrestrial realm (Faith, 1992; Rosauer et al., 2009; Safi et al., Distribution data and phylogenetic reconstruction 2013; Jetz et al., 2014; Zupan et al., 2014; Daru et al., 2015; Guilhaumon et al., 2015). Despite the growing interest in inte- We compiled data on the global distribution of all 72 seagrass grating taxonomic and phylogenetic methods for the assessment species and 55 (of 70) mangrove species from the IUCN Red of biodiversity (Devictor et al., 2010; Mishler et al., 2014; Zupan List database extent of occurrence maps (EOO) (http:// et al., 2014; Daru et al., 2015), phylogenetic metrics have not www.iucnredlist.org/technical-documents/spatial-data). These been implemented in conservation planning for marine species. maps have been extensively assessed and updated, providing While the selection of hotspots based solely on the top grid cells accurate presence/absence data at the scale of 1° × 1° grids (c. for each metric could ensure protection of certain habitats, this 110 km × 110 km), a resolution commonly used in global-scale approach may be inefficient (and even ineffective) for maxim- macroecological studies (e.g. Storch et al., 2012). izing protection of biodiversity (Daru et al., 2015). Complemen- tarity methods, which aim to include the maximum number of Phylogenetic reconstruction and divergence time estimation for unrepresented species or phylogenetic branch lengths with each seagrass species new location conserved,